Review Article Ion Transporters and Abiotic Stress Tolerance in Plants

14 Pages·2014·1.24 MB·English

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ISRNMolecularBiology
Volume2012,ArticleID927436,13pages
doi:10.5402/2012/927436
Review Article
Ion Transporters and Abiotic Stress Tolerance in Plants
Fa¨ıc¸alBriniandKhaledMasmoudi
PlantProtectionandImprovementLaboratory,CentreofBiotechnologyofSfax(CBS),UniversityofSfax,
P.O.Box1177,3018Sfax,Tunisia
CorrespondenceshouldbeaddressedtoFa¨ıc¸alBrini,[email protected]
Received15March2012;Accepted10April2012
AcademicEditors:M.Greenwood,T.O’Connor,andM.Sekine
Copyright©2012F.BriniandK.Masmoudi.ThisisanopenaccessarticledistributedundertheCreativeCommonsAttribution
License,whichpermitsunrestricteduse,distribution,andreproductioninanymedium,providedtheoriginalworkisproperly
cited.
AdaptationofplantstosaltstressrequirescellularionhomeostasisinvolvingnetintracellularNa+andCl−uptakeandsubsequent
vacuolarcompartmentalizationwithouttoxicionaccumulationinthecytosol.Sodiumionscanenterthecellthroughseverallow-
andhigh-affinityK+carriers.SomemembersoftheHKTfamilyfunctionassodiumtransporterandcontributetoNa+removal
fromtheascendingxylemsapandrecirculationfromtheleavestotherootsviathephloemvasculature.Na+sequestrationintothe
vacuoledependsonexpressionandactivityofNa+/H+antiporterthatisdrivenbyelectrochemicalgradientofprotonsgenerated
bythevacuolarH+-ATPaseandtheH+-pyrophosphatase.Sodiumextrusionattheroot-soilinterfaceispresumedtobeofcritical
importanceforthesalttolerance.Thus,averyrapideffluxofNa+fromrootsmustoccurtocontrolnetratesofinflux.TheNa+/H+
antiporterSOS1localizedtotheplasmamembraneistheonlyNa+effluxproteinfromplantscharacterizedsofar.Inthispaper,we
analyzeavailabledatarelatedtoiontransportersandplantabioticstressresponsesinordertoenhanceourunderstandingabout
howsalinityandotherabioticstressesaffectthemostfundamentalprocessesofcellularfunctionwhichhaveasubstantialimpact
onplantgrowthdevelopment.
1.Introduction processes such as photosynthesis. The osmotic component
of salinity is caused by excess inorganic ions such as Na+
Agriculturalproductivityisseverelyaffectedbysoilsalinity. and Cl− in the environment that decrease the osmotic
Environmental stress due to salinity is one of the most potential of the soil solution and hence water uptake by
serious factors limiting the productivity of agricultural theplantroot.UptakeofabundantlyavailableNa+ andCl−
crops, most of which are sensitive to the presence of high therefore, offers a comparatively cheap way to lower the
concentrations of salts in the soil. There are two main tissue-osmotic potential. To avoid the risk of ion toxicity
components to salinity stress in plants; an initial osmotic associated with this strategy, Na+ and Cl− are generally
stress and a subsequent accumulation of toxic ions which compartmentalized in the vacuole and/or in less sensitive
negatively affects cellular metabolism [1]. In addition, it tissues.Inparallel,adjustmentofthecytoplasmiccompart-
canleadtosecondarystressessuchasnutritionalimbalance ment is achieved via production of compatible osmolytes
and oxidative stress [2]. The Na+ cation is chaotropic suchas,proline,mannitol,sorbitol,andglycinebetaine.The
and predominantly associated with the deleterious effect of latter also acts as antioxidant and thus detoxifies reactive
salinity, and therefore, most research has focused on this oxygen species (ROS). However, when plants are growing
mineral.However,plantadaptationtosaltstressalsorequires in high salt concentrations, an adequate sequestration of
appropriate regulation of Cl− homeostasis [3]. Indeed, for ions in the vacuole can become a limiting factor, especially
species such as soybean, citrus, and grapevine where Na+ in the case of glycophytes. In this scenario, plants can
is predominantly retained in the roots and stems, Cl− is accumulate excessive amount of Na+ in the cytosol which
consideredmoretoxicsincethisionisaccumulatedtohigh negatively affects many aspects of cellular physiology. The
levels in shoot tissues, negatively impacting on essential most abundant inorganic cation in the cytosol is K+, in
2 ISRNMolecularBiology
plant as in animal cells. This might be due to the fact 2.SodiumUptakefromSoil
that this cation is less chaotropic than Na+, that is, more
The excess of salts in the soil solution poses a challenge
compatible with protein structure even at high concentra-
tions. The physicochemical similarities between Na+ and to the plant. Na+ and other ions taken up by roots are
transportedtoshootsinthetranspirationstream,wherethey
K+ lead to a competition at transport and catalytic sites
accumulate over time [3]. Elevated concentrations of salts
thatnormallybindtheessentialcationK+ andmaintaining
arebuiltupintheapoplastandeventuallyinsidethecell,as
a high cytosolic K+/Na+ ratio is believed to improve salt
waterevaporates.Theaccumulationofionsinplanttissues
tolerance[4,5].Oxidativestressisanotheraspectofsalinity
results in progressive damage. These ionic specific stress
stress which is in fact a consequence of salinity-induced effectsaresuperimposedonthosecausedbyhyperosmolarity
osmotic and/or ionic stress [6]. The salt-induced produc-
[3].Whetherplantshavespecifictransportsystemsforlow-
tion of ROS such as superoxide radicals (O2−), hydrogen affinityNa+uptakefromsoilremainsanopenquestion[16]
peroxide (H2O2), and hydroxyl radicals (OH) has then a andtheexactmechanismsresponsibleforrootNa+ andCl−
severeeffectoncellularstructureandmetabolismnegatively
uptakeareonlypartiallyclearandlikelyincludetransporters
[7]. fromseveralgenefamiliesandtransportclasses.
Although considerable progress was made to increase
and secure crop yield through conventional breeding, the
2.1.TheRoleofNonselectiveCationChannelsinNa+ Uptake.
goal of improving the resistance of crops to abiotic stresses
In the last few years, evidence has been presented support-
hasseenlimitedsuccessbecauseofthecomplex,multigenic
ing the existence of weakly voltage-dependent nonselective
natureofthetraits,andthenarrowgeneticvariationinthe
cation channels (NSCC) that are the main pathway for
gene pools of major crops. Numerous genes and proteins Na+ entry into the roots, at high soil NaCl concentrations
have been shown to affect the tolerance to environmental
[17, 18]. Although there are many candidate genes in the
stress in an array of plant species, which together compose databases that could encode these NSCC channels, their
a complex puzzle with a myriad of individual elements identityremainselusive.Twofamiliesofnonselectivecation
and crisscrossing signal transduction pathways. A common channels, CNGCs (cyclic nucleotide-gated channels) [19],
theme of tolerance is the adequate control of salt uptake and GLRs (glutamate-activated channels) [20] have been
at the root level, regulation of influx into cells, control suggested to be candidate NSCC channels (Figure1) [17].
over long distance transport, and the compartmentation TheinhibitionofNa+influxandNSCCcurrentsuponaddi-
at both cellular and tissue levels [8, 9]. These processes tion of membrane permeable cyclic nucleotide analogues
are mediated by membrane transporters and manipulat- provided correlative evidence for the operation of CNGCs
ing the activity of this class of proteins has therefore inplants[21],afamilyofplantchannelsthatinArabidopsis
enormous potential to affect plant performance in saline comprise20members[22].Todate,fiveAtCNGCshavebeen
conditions [10]. Different approaches have been used to characterized(AtCNGC1,2,3,4,and10)[19,23–25].Elec-
identify membrane transporters with putative functions in trophysiological studies have suggested that AtCNGC1 and
salt tolerance. Yeast is widely used as host for heterolo- AtCNGC4 are equally permeable to K+ and Na+ and when
gous expression of plant proteins. Yeast complementation expressed in Xenopus oocytes, they displayed activation by
screens led to the isolation of plant transporters such as cyclicnucleotides[19,23].AtCNGC2appearstobeselective
the vacuolar Na+/H+ antiporter AtNHX1 [11] and the for K+ and to discriminate against Na+ [19]. AtCNGC10
plasmamembraneK+/Na+ symporterTaHKT1[12].Lossof rescuedK+ transportdefectivemutantsofE.coli,yeast,and
function mutants in the model system Arabidopsis thaliana Arabidopsisakt1-1,suggestingthatAtCNGC10mediatesthe
helpedcharacterizemanymembranetransportersincluding transport of K+ into the roots [24]. AtCNGC3 was recently
AtHKT1:1involvedinlongdistanceNa+ transport[13],the characterized by functional complementation of yeast and
plasma membrane Na+/H+ antiporter SOS1 [14], and the bycharacterizationofArabidopsisT-DNAknockoutmutants
vacuolar pyrophosphatase AtVP1 [15]. It is well established [25]. AtCNGC3 was primarily expressed in the cortical and
that uptake, efflux, translocation, and compartmentation epidermalrootcells.Growthofthemutantseedlingsintoxic
of toxic ions (mainly Na+ and Cl−) provide important NaCl (and KCl) concentrations was improved, suggesting a
bases for salinity tolerance in plants, and hence, a potential restricted ion influx in the mutant plants [25]. Ionotropic
avenuetoimprovecrops.However,alackofunderstanding glutamate receptors (GLRs) are proteins that interact with
regardingthemolecularentitiesandcomplexinteractionsof glutamate and form cation channels with a wide range of
the responsible membrane transport proteins has hindered permeability’s. In Arabidopsis, the family of putative GLRs
progress in this respect. The present paper focuses on the comprises 20 members [20]. Glutamate-activated Na+ and
main ionic constituents of salinity, Na+ and Cl− and also Ca2+ voltage-independent currents were characterized in
analyses which specific membrane transporters have been Arabidopsisroots.Demidchiketal.[20]notedthatalthough
shown,or arebelieved, tobe involved in uptake,extrusion, theeffectsofenvironmentalfactorsonapoplasticglutamate
long-distancetransport,andcompartmentalizationofsaltat remain unclear, the concentrations of glutamate required
thecellularandtissuelevel.Subsequently,thepapercritically for half activation of these channels correlated well with
evaluatesthereporteddatatoassesswhichproteinsmaybe the range of apoplastic glutamate concentrations reported
particularly suitable as engineering targets to improve crop (0.2–0.5mM), suggesting a role of these channels in Na+
salttolerance. uptake.
ISRNMolecularBiology 3
mb Cytoplasm
External medium
H+ ATPase H+pump: membrane energisation:
electrical gradient and pH gradient
AATTPP
P
T
A
NHa++ Antiporter Na+/H+antiporters TPase
A
P
Na+ + i
H
NHX
H+ H+ H+PPase
Vacuole
Channel activity including
Na+? K+ Channel
NSCC channels
CNGC channels?
K+,Na+,
(Mg2+,Ca2+) Transporter HKT transporters Na+ HKT1
Figure1:Themaintransportsystemsidentifiedsofarattheplasmamembrane.
2.2. Potassium Channels May Contribute to Na+ Uptake. [30]. Members of the HKT gene family are Na+-specific
Sodium has a strong inhibitory effect on K+ uptake by transporters(althoughtheywereinitiallydescribedashigh-
cells,presumablybyinterferingwithtransportersintheroot affinityK+ transportersandhencetheirname)thatmediate
plasma membrane such as the Shaker type K+ channels eitherpreferentialNa+ transportorNa+-K+ symport,partly
(KAT1andAKT1formthepredominantinwardK+conduc- depending on whether the specific transporter has a highly
tanceobservedinplantplasmamembranes).Suchchannels conserved serine (subfamily 1) or glycine (subfamily 2)
generally have a high K+/Na+ selectivity and were generally residueinthefirstporeloopoftheproteinandontheextra-
regarded not to play a significant role in Na+ [26, 27]. cellularNa+-K+ ratio[31,32].Generally,HKT membersof
However, a more recent work suggests that the picture is subfamily 1 have a relatively higher Na+-to-K+ selectivity
morecomplexandtheremaybeecophysiologicalvariations than subfamily 2 HKT transporters. In Arabidopsis, loss of
in this respect. Wang et al. [28] used apharmacological function of the only HKT1;1 gene encoding a Na+-selective
approach to characterize Na+ uptake in the halophyte transporter caused the accumulation of Na+ in leaves but
Suaeda maritima and concluded that the low-affinity Na+ reducedNa+concentrationsinroots,withlittleeffectonthe
uptakepathwayin this speciesresemblesanAKT1channel. netuptakeofNa+bytheplant[13,33,34].AtHKT1;1ispref-
Similarly, Kader and Lindbergh [29] provide evidence that erentiallyexpressedinthevasculature,whereitisthoughtto
K+channelsmediatesubstantialNa+influxinasalt-sensitive regulatetheNa+ distributionbetweenrootsandshoots[13,
rice cultivar but not in a tolerant one. In both cases the 31–35]. Two complementary functions for AtHKT1;1 have
conclusions were derived from applying channel blockers beenproposed[36].Thephloemrecirculationmodelposits
and inhibitors which can be notoriously nonspecific, but that Na+ is loaded into shoot phloem cells by AtHKT1;1
these findings do suggest that K+ channels are potential and then transferred to roots via the downward stream
pathways for root Na+ influx. In addition, the study by of phloem, preventing Na+ over accumulation in shoots
Wang et al. [28] suggests that basic processes such as Na+ (Table1)[37].However,thereseemstobelittle(10%orless)
uptakemaybeconsiderablydifferentinhalophytesandsuch retranslocation of Na+ from leaves via the phloem relative
diversitycouldbeanimportantcontributortosalttolerance. totheamountimportedinthetranspirationstreamviathe
However,thescarcityindatafromhalophytesinthisrespect xylem[17,38,39].Ontheotherhand,AtHKT1;1isgenerally
formsalargehindranceintestingthishypothesis. accepted to mediate the retrieval of Na+ from the xylem
sap, thereby restricting the amount of Na+ reaching the
2.3. Carrier-Type Transporters That Mediate Na+ Uptake. photosynthetictissues[34,37–39].ThesetwoNa+transport
HKTs (high affinity potassium transporters) are carrier- processes could be functionally linked to achieve basi-petal
typeproteinsthatmediateNa+ andK+ transport(Figure1) translocation of Na+ because ions that were unloaded by
4 ISRNMolecularBiology
Table1:Plantiontransportersinvolvedinsalttoleranceidentifiedbyfunctionalanalysis.
Source Identification
Name Geneproduct Function Harbourgspecies Reference
species method
Sodiuminflux
AtHKT1 A.thaliana Na+transporter Na+/K+homeostasis Mutation Arabidopsis [13]
Na+/K+
HKT1 T.aestivum K+/Na+homeostasis Overexpression Wheat [31]
transporter
Sodiumefflux
Plasmamembrane
AtSOS1 A.thaliana Na+detoxification Mutation Arabidopsisoverexpression [76]
Na+/H+antiporter
Plasmamembrane
TaSOS1 T.aestivum Na+detoxification Mutation Arabidopsisoverexpression [99]
Na+/H+antiporter
Sodiumcompartmentation
VacuolarNa+/H+ Arabidopsis, [11]
AtNHX1 A.thaliana Na+vacuolarsequestration Overexpression
antiporter Cabbage,tomato [93]
VacuolarNa+/H+
TNHX1 T.aestivum Na+vacuolarsequestration Overexpression Arabidopsis [96,114]
antiporter
H+transport,vacuolar
AVP1 A.thaliana VacuolarH+-PPase Overexpression Arabidopsis [15]
acidification
H+transport,vacuolar
TVP1 T.aestivum VacuolarH+-PPase Overexpression Arabidopsis [96,114]
acidification
Regulatorygenes
Serine/threonine
SOS2 A.thaliana SOS1regulator Mutation Arabidopsis [87]
Proteinkinase
Ca++binding
SOS3 A.thaliana Ca++sensor/SOS2activator Mutation Arabidopsis [81]
protein
xylem parenchyma cells might be transported into the [43].Thus,itappearsthatOsHKT2;1augmentsmonovalent
phloemviasymplasticdiffusion[36].Engineeredexpression cation uptake by providing high-affinity Na+ uptake in
of AtHKT1;1 in the root pericycle of Arabidopsis enhanced K+ deficient conditions. However, OsHKT2;1 relevance in
inward Na+-transport in the targeted cells, reduced root- Na+ uptake during salinity stress may be limited since
to-shoot transfer of Na+, and improved salt tolerance [40]. it has a micromolar affinity for Na+, and its activity is
However, it remains unclear whether the reduced activity rapidly downregulated at higher ambient concentrations
of AtHKT1;1 was the sole basis for enhanced tolerance or of Na+. Similar high-affinity Na+ uptake was observed
if there were other processes that could also contribute to in K+-starved barley roots. However, when heterologously
salttolerancelinkedtoenhancedNa+ accumulationsuchas expressed in yeast, HvHKT2;1 was shown to mediate Na+
improved capacity for Na+ sequestration in vacuoles [41]. (or K+) uniport, Na+-K+ symport, or a combination of
Similar studies in cereals have shown that natural variation both,dependingontheconstructfromwhichthetransporter
in the activity or expression of HKT transporters may be was expressed [30, 46]. These characteristics suggest that
a genetic resource for enhanced NaCl tolerance. In rice, the HKT transporters are potentially of importance in the
two of the nine members, OsHKT2;1 and OsHKT2;2, are regulationofNa+influxintoroots.SeveralQTLsresponsible
expressed in roots amongst other tissues [42]. OsHKT2;2 for variation of K+ and Na+ content were mapped to HKT
catalyses Na+-dependent K+ uptake [43]. OsHKT2;1 has family genes. QTLs analyses showed that greater shoot K+
been shown to catalyse high-affinity Na+ uptake into roots contentoftherelativelysalt-tolerantricecultivarNonaBokra
underK+-starvationconditions,anditappearsthatNa+can cosegregatedwiththepresenceofanallelicvariantofSKC1
partially replace the function of K+ under such conditions (shoot K+ content) with greater activity relative to that of
[43]. OsHKT2;1 has been shown to catalyse high-affinity the salt-sensitive Koshihikari variety [47]. SKC1 (renamed
Na+ uptake into roots under K+-starvation conditions, and OsHKT1;5) is a plasma membrane K+-independent, Na+-
it appears that Na+ can partially replace the function of selective transporter that is preferentially expressed in the
K+ under such conditions [43]. Expression of OsHKT2;1 is parenchymacellssurroundingxylemvessels.ThegreaterNa+
localized to the root epidermis, cortical cells, and vascular concentrationinthexylemsapandleavesofthesalt-sensitive
tissues of both roots and leaves [43–45], and expression variety would be a consequence of a weaker SKC1 allele
patterns in roots were found to be different in salt-tolerant andreducedNa+reabsorptionfromthexylem.Quantitative
and sensitive varieties in response to NaCl stress [44]. geneticanalysesinwheathavealsoledtotheidentificationof
Loss of function mutants in OsHKT2;1 shows reduced twoloci,Nax1andNax2,whichreducedNa+ accumulation
growth in low K+ conditions and accumulated less Na+ in the leaf blade by excluding Na+ from the xylem by two
ISRNMolecularBiology 5
different mechanisms [38]. The process controlled by Nax2 very little is clear about the molecular mechanisms behind
was confined to the roots and had the effect of reducing the substantial Cl− influx that results from salinization [9].
the transport of Na+ from root to shoot, presumably by Genes and proteins involved in Cl− transport have been
improved discrimination between Na+ and K+ at the point verypoorlystudiedinplants.Theattentionhasbeenmainly
of xylem loading. The Nax1 locus enhanced the retention focused on the voltage-dependent Cl− channel CLC family
ofNa+ intheleafsheath,thusrestrictingfurtherpassageto [63–65]. Phylogenetic and functional analyses have shown
theleafblade[38].High-resolutionmappingandsequencing that plant CLC genes encode anion channels and active
analysesofknownNa+transportergeneshavesuggestedthat Cl−/H+ antiporters localized in endosomal compartments,
the Nax1 and Nax2 loci are attributable to polymorphisms whichareinvolvedinNO3− compartmentalization[66]and
in wheat HKT genes encoding proteins of the subfamily 1 pH regulation in the trans-Golgi system [67]. Although
withpreferredNa+transport[48,49].Theseresultsstrongly the transcript abundance of several CLCs is affected by
indicate that Na+ exclusion from the transpiration stream salinity [68], they are unlikely to contribute to root Cl−
may be an important mechanism in the salt tolerance of uptake: Firstly, plant CLCs have only been detected at
cereals, similar to many other plant species [17]. It should endomembranes which appear to exclude a role in Cl−
bepointedout,however,thatmoststudiesconcerningQTL uptake and secondly the thermodynamics of Cl− uptake
analysisforsalttolerancearebasedinNa+and/orK+content roleoutpassive-channel-typemechanisms.Asecondclassof
intissuesororgansandnotdirectlyinsalttolerance.Often, potential Cl− transporters is formed by the cation chloride
higher Na+/K+ ratios are regarded as determinants of salt cotransporters (CCCs) encoding one gene in Arabidopsis
tolerance itself without considering any other agronomical and two genes in rice. The Arabidopsis thaliana cation-
orphysiologicaltraits.In fact,the SKC QTLofricedid not Cl− cotransporters (AtCCCs), expressed in root and shoot
showasignificantcorrelationcoefficientwithsurvivaltosalt tissues, mediate the coordinated symport of K+, Na+, and
stress[50].AcleardifferenceshouldbemadebetweenQTLs Cl− and have been postulated to participate in the long-
responsible of ionic balance and QTLs for salt tolerance. distance transport of Cl− [62]. Loss of function of AtCCC
In addition to HKTs, other carriers have been implicated inArabidopsisledtoachangedroot:shootCl−ratiobutalso
in Na+ uptake. Some members of the high-affinity K+ to a large increase in net Cl− uptake arguing against a role
uptaketransporterfamilyHAK/KUP/KTmaytransportNa+ of AtCCC in the uptake of this ion [62]. More recently, the
with low affinity in the presence of high Na+:K+ ratios Arabidopsisslowanionchannelassociated1(AtSLAC1)gene
was shown to encode for the guard cell plasma membrane
[51].Furthermore,yeastexpressionstudiesrevealedthatthe
normalfunctionofHAK/KUP/KTs,high-affinityK+ uptake, S-type anion channel involved in stomatal closure [69, 70].
Anothermemberofthisfamily,AtSLAH1,isexpressedinthe
iscompetitivelyinhibitedbyNa+,pointingtoasharedtrans-
root vasculature suggesting a potential involvement in the
portpathwayofthetwomonovalentcations[52,53].Several
long-distanttransportofanions[69].
studieshaveshownsubstantialtranscriptionalregulationof
HAK/KUP/KT isoformsbysaltstress[54–56].Forexample,
Suetal.[57]observedthattheexpressionofHAKsinMesem- 3.TransportersInvolvedinSaltEfflux
bryanthemumcrystallinumwasupregulatedduringsaltstress
and K+-starved conditions. However, whether this result It is essential that plants possess adequate efflux systems
and those for other HAKs relate to a potential role in Na+ to remove potentially dangerous ions such as Na+ from
uptake or augmentation of K+ uptake during salinity stress the cytosol. Inevitably, the mechanisms to extrude Na+
remainstobeestablished.Thelow-affinitycationtransporter into the apoplast or vacuole have to be energized which
typically occurs via H+-coupled antiport [5, 71], whereas
LCT1 from wheat functions as nonselective cation carrier
conducting K+, Rb+, Na+, and Ca2+ transport in yeast [58, those for Cl− may be (partially) passive. Early studies on
59].ExpressionofLCT1inyeastleadstoanincreaseincation tonoplast antiporters showed significant upregulation of
influxandhypersensitivitytoNa+[60].Additionofexternal their pumping capacity after plant exposure to salt [72,
Ca2+ wasfoundtoreduceNa+ influxandsensitivity,butthe 73]. In the plasma membrane too, evidence for H+:Na+
cation profile of the influx caused by LCT1 resembled that antiporters was obtained underlining the relevance of such
of endogenous ion transport in yeast, suggesting that LCT1 systems to plant salt tolerance [74]. Data dealing with Cl−
might be stimulating the ion transporters already present efflux are scarce: using compartmental flux analysis, Britto
[60]. and Kronzucker [75] showed large Cl− efflux when plants
were exposed to 100mMNaCl. Just as is the case for Na+,
2.4. Transporters Involved in Cl− Uptake. Chloride (Cl−) is the majority (up to 90%) of Cl− that entered the symplast
a majorosmotically activesolutein thevacuoleinvolved in wasquicklyremoved.AlthoughsomeoftheCl−effluxcould
bothturgorandosmoregulationprocesses[61],withimpli- theoretically be mediated by anion channels, no data are
cations for the proper development of plants [62]. Despite available regarding the mechanistic details or regarding the
itsimportanceinplantbiology,Cl−isoneofthelessstudied identityoftheproteinsinvolved.
essentialnutrientsatthephysiologicalandmolecularlevels.
In contrast to Na+, Cl− uptake in most conditions must 3.1. Na+ Efflux Mechanisms at the Plasma Membrane.
be energized, but although there is a substantial amount Comparisons of unidirectional Na+ fluxes and rates of net
of information regarding K+ and Na+ transport in plants, accumulation of Na+ in roots indicate that 70–95% of the
6 ISRNMolecularBiology
Na+ fluxed into the root symplast is extruded back to the 3.2. Sodium Compartmentation: The Vacuolar Na+/H+
apoplast,andthatsmalldifferencesinNa+exclusioncapacity Antiporter and the H+ Pump. The compartmentation of
leadtomajorchangesinthenetaccumulationofNa+ [17]. Na+ ions into vacuoles provides an efficient mechanism
In Arabidopsis, the plasma membrane Na+/H+ exchanger to avert the toxic effects of Na+ in the cytosol. The
SOS1(SaltOverlaySensitive)facilitatesNa+ homeostasisby transportofNa+ intothevacuolesismediatedbycation/H+
extruding the ion from root epidermal cells at the root-soil antiporters that are driven by the electrochemical gradient
interface (Table1, Figure1) [76, 77]. SOS1 is preferentially of protons generated by the vacuolar H+-translocating
expressedinxylemparenchymacells,andanalysesoftheNa+ enzymes, the H+ ATPases and the H+ pyrophosphatase
root/shootpartitioninginrootsofsos1plantsunderdifferent (H+-PPase) (Table1, Figure1). Although the activity of
saltregimesindicatethatSOS1participatesintheredistribu- these cation/H+ antiporters was demonstrated more than
tion of Na+ between the root and shoot, likely working in
20yearsago[72],theirmolecularcharacterizationwasonly
concert with AtHKT1;1 at the plasma membrane of xylem
possible after the Arabidopsis genome-sequencing project.
parenchyma cells [34, 36, 76, 78]. Additional evidence of
Na+ compartmentation in the vacuole occurs in all tissues
the involvement of SOS1 in long-distance Na+ transport
andisanimportantmechanismforosmoticadjustmentand
has been produced recently in the halophytic Arabidopsis
Na+ detoxificationinthecytosol.ThereareeightNHX gene
relative Thellungiella salsuginea (a.k.a. T. halophila) and in
family members in Arabidopsis [89], and the functions of
tomato [79, 80]. Lower net Na+ flux was observed in the
AtNHX1, 4, 7 and 8 have been studied. AtNHX7 is also
xylem sap of tomato plants with suppressed SOS1 activity
known as AtSOS1 and AtNHX8 has been shown to be a
[80]. Downregulation of ThSOS1 in Thellungiella increased
Na+ accumulationintheroottipandinthestele.Maximal Li+/H+ antiporter [90], although the biological relevance
Na+ accumulation, concomitant with a decrease in the K+ of Li+ transport remains obscure. AtNHX4 is localized to
content, was found in the root xylem parenchyma. These the vacuole and might function in concert with AtNHX1
cells presented a Na+-K+ ratio more than 12 times higher (Table1) [91]. Several reports indicate that constitutive
than equivalent cells in wild-type plants. Reduced or abol- overexpressionofthevacuolartransportersincreasesthesalt
ishedactivityofSOS1interfereswithK+nutritionandlong- toleranceofavarietyorspecies.Constitutiveoverexpression
distance transport [80]. Mutations in rice and Arabidopsis of the Arabidopsis vacuolar Na+/H+ antiporter, AtNHX1,
HKT Na+ transporters also reduce K+ accumulation in appears to increase salinity tolerance significantly in yeast
shootsduringsaltexposure[34,47].TheactivityoftheSOS1 [92],Arabidopsis[11],tomato[93],Brassicanapus[94],and
exchanger is regulated through protein phosphorylation by cotton[95].Similarly,constitutiveoverexpressionofvarious
the SOS2-SOS3 kinase complex in Arabidopsis (Table1) cereal homologs has been reported to improve the salinity
[77, 81]. SOS2/CIPK24 is a serine/threonine protein kinase tolerance of Arabidopsis [96], rice [97, 98], wheat [99],
of the SnRK3/CIPK family. SOS3/CBL4 is a myristoylated and barley [100]. The overexpression of NHX1 appears to
membraneboundCa2+ sensorbelongingtotherecovering-
increasethecapacityoftheplanttoregulatecytoplasmicand
likefamilyofSCaBPs/CBLs.UponCa2+binding,SOS3binds
vacuolarpH[101,102].Thecationselectivityisregulatedby
to and enhances the protein kinase activity of SOS2 [82].
aluminalC-terminus[103].TheoverexpressionofNHX1in
Besides activating SOS2, SOS3 was shown to recruit SOS2
ArabidopsisledtoasmallincreaseinshootNa+accumulation
totheplasmamembranetofacilitateinteractionwithSOS1
[11], possibly allowing the cells to maintain a favourable
[81]. SOS2 also interacts with SCaBP8/CBL10 to form an
osmoticbalance,yetmaintaininglowcytoplasmicNa+levels
alternative protein kinase complex that regulates SOS1 at
duetosequestrationoftheNa+withinthevacuole.Thenhx1
the plasma membrane [83]. SOS2 has recently been shown
mutanthadsignificantlylowerNa+/H+andK+/H+exchange
to phosphorylate SCaBP8/CBL10 at its C-terminus [84],
capabilitiesinisolatedvacuoles,fewerlargeepidermalcells,
thus adding a new layer of regulation to CBL proteins
besides Ca2+ binding and fatty acyl modifications [85]. and less overall leaf area, indicating that NHX1 also plays
a developmental role [104]. Overexpression and knockout
This phosphorylation was induced by salt stress, occurred
at the membrane, stabilized the SCaBP8-SOS2 interaction, of the NHX1 gene in Arabidopsis have been shown to
and enhanced plasma membrane Na+/H+ exchange activ- significantlyanddifferentiallyaltertheexpressionofalarge
ity [84]. Surprisingly, interaction of SOS2/CIPK24 with number of genes involved in the response to salt stress,
SCaBP8/CBL10 mayalso resultin localization of the kinase indicating that Arabidopsis can respond to a change in one
complex at the vacuolar membrane where it mediates salt Na+ transporterbyregulatingothergenes[105,106].Other
tolerance by regulating the accumulation of Na+ in shoot membersoftheNHXfamilyarealsocapableofmovingNa+.
tissues by an as yet undefined mechanism that may involve Yokoi et al. [89] reported that AtNHX2 and AtNHX5 could
regulationoftheNa+/H+exchangeatthetonoplast[86,87]. be important salt-tolerant determinants and observed that
RegulationofthetonoplastV-ATPasebySOS2intheabsence AtNHX2hasamajorfunctioninvacuolarNa+sequestration.
of CBL proteins has also been reported [88]. Presumably, H+ pumpsintheplasmamembraneandtonoplastenergize
the posttranslational modifications of SCaBP8/CBL10 or solute transport necessary to compartmentalize cytotoxic
the interaction of combinatorial protein kinase complexes ionsawayfromthecytoplasmandtofacilitatethefunctionof
with specific targets in different cellular membranes may ionsassignaldeterminants[107–109].Thatisthesepumps
ultimately define the localization of the protein kinase in provide the driving force (H+ electrochemical potential)
vivo. for secondary active transport and function to establish
ISRNMolecularBiology 7
membranepotentialgradientsthatfacilitateelectrophoretic in both leaves and roots, showed transcript reduction in
ion flux. The plasma membrane localized H+ pump is a P- thechlorideaccumulatingsalt-sensitiveIR29whiletransient
typeATPaseandisprimarilyresponsibleforthelargepHand inductionoccurredinthechlorideexcludingvarietyPokkali
membranepotentialgradientacrossthismembrane[109].A [118]. Die´dhiou and Golldack [68] showed a coordinated
vacuolar type H+-ATPase and H+-PPase generate the ΔpH regulation of anion and cation homeostasis in salt-treated
andmembranepotentialacrossthetonoplast[108,110].The riceandsuggestedafunctionforOsCLCcinosmoticadjust-
activity of these H+ pumps is increased by salt treatment, mentathighsalinity.Nakamuraetal.[119]showedthatthe
and induced gene expression may account for some of the same CLC channels partially complimented the yeast gef1
upregulation [108, 111]. The H+-PPases are considered to
mutantwhichlacks theyeastCLC channel. In conjunction,
form a multigene family. Two cDNA clones (OVP1 and
these findings suggest that CLC-type anion channels are
OVP2)encodingvacuolarH+-PPasesisolatedfromricewere importantinmediatingCl−sequestrationinvacuole.
reported [112]. Indeed, there are two genes in Arabidopsis
annotated as inorganic pyrophosphatase H+-PPase (AVP1,
4.Long-DistanceTransportofNa+
AVP3) and a third loci encoding a pyrophosphatase like
(AVP2=AVPL1),morethanfiveisoformsinrice,andatleast
An important issue in salt stress physiology is Na+ translo-
threeisoformsinbarley[107,113].
cation from the root to the shoot [120, 121]. Physiological
Ithasbeenpreviouslydemonstratedthatoverexpression
evidence suggests that halophytes and salt-resistant glyco-
of the H+-PPase AVP1 increases salinity tolerance and Na+
phytes actively transport Na+ from the root to the shoot,
accumulation in Arabidopsis [15]. The vacuolar Na+ levels
whereassalt-sensitiveglycophytesappeartolimitNa+ entry
ofthetransformantswerefoundtobehigherthanthoseof
intothetranspirationalstreamtopreventNa+accumulation
wild-typeplants,indicatingthatoverexpressionofAVP1led
in the shoot [120, 121]. The transporter(s) responsible for
to increased activity of the Na+/H+ antiporter. Functional
Na+ transporttoandfromthexylemvesselsarenotknown,
characterization of wheat Na+/H+ antiporter TNHX1 and
although plasma membrane Na+/H+ antiporters have been
vacuolarpyrophosphataseTVP1wasreportedbyBrinietal.
proposed to fulfil this role [111, 122]. It also is not known
[114]. Transgenic Arabidopsis lines overexpressing TNHX1
whichcelllayer(s)mightbecriticalforcontrollingtheextent
or TVP1 are much more resistant to high concentrations
ofNa+ entryorexitfromthexylem.Theplasmamembrane
of NaCl and to water deprivation than the wild-type
antiporter SOS1 is expressed in root parenchyma and in
plants.Thesetransgenicplantsgrowwellinthepresenceof
Arabidopsis impacts on Na+ loading into the xylem sap
200mMNaCl and also under a water-deprivation regime,
duringmoderatesaltstress[76].However,itsexactfunction
while wild-type plants exhibit chlorosis and growth inhi-
maydependontheseverityofthesalinitystressandincludes
bition [96]. In barley, expression of the H+-PPase HVP1, removal of Na+ from the xylem stream when salt stress is
and the vacuolar Na+/H+ antiporter NHX1, was similarly
excessive. In Arabidopsis, loss-of-function mutations in the
upregulated by salt stress [100] and is regulated by ABA, HKT1 gene lead to overaccumulation of Na+ in shoots and
auxin,andgibberellin[115].Thesimultaneousexpressionof rendered the plant Na+ hypersensitive [37, 123]. RNA in
NHX and AVP genes in rice was found to increase salinity situ hybridizations showed that HKT1 is expressed mainly
tolerance to a greater extent than expression of the genes in leaf phloem tissues and mediates Na+ loading into the
individually [98]. The overexpression of AVP1 also appears phloem vessels. In addition, HKT1 may be involved in Na+
toincreasegrowthratesofplantsduetoaninteractionwith unloading from the phloem sap in roots thus providing a
theauxintransporterPIN1,whichincreasesauxintransport mechanismforNa+retranslocationfromshoottoroot[37].
resulting in more robust plants which are better able to In rice, OsHKT1;5 is a plasma membrane Na+ transporter
survivestressconditions[24,116]. expressedinxylemparenchymacellsthatretrievesNa+from
the xylem sap [47]. Genetic analysis revealed an important
3.3.RoleofCl−ChannelsinVacuolarCl−Compartmentation. K+-homeostasis QTL called SKC1 [50]. The SKC1 gene
InadditiontoNa+,Cl−compartmentationisalsoimportant was cloned and found to be OsHKT1;5 [50]. Heterologous
forsalttolerance,aselevatedlevelsofCl−inthecytosolmay expressionrevealedthatOsHKT1;5isaNa+transporter,and
be harmful, particularly in the case of citrus crops [117]. whole plant analysis indicated that it functions in the root
Sincethevacuoleismoderatelypositivewithreferencetothe xylem parenchyma to retrieve Na+ from the xylem stream,
cytoplasm,partofthevacuolarCl−sequestrationcouldpro- thereby reducing Na+ accumulation in the shoot [50]. Flux
ceed through ion channels, and several voltage-gated anion analysis of a salt-tolerant durum wheat landrace, line 149,
channelsoftheCLC familyhavebeendetectedinthetono- revealed that Na+ exclusion in this line is underpinned by
plast of various species. In Arabidopsis, CLCa was recently the individual traits of decreased Na+ transfer to the shoot
shown to function primarily as a H+-coupled antiporter and increased Na+ retrieval to the leaf sheath tissue [124].
to drive vacuolar nitrate accumulation [66], whereas CLCc Nax1andNax2,twopreviouslymappedQTLsthathavebeen
may also be involved in NO3− homeostasis rather than linkedtosalinitytoleranceinline149werefoundtocontrol
vacuolar Cl− sequestration. However, CLC transcription thetwotransporttraits[38].TheNax2locuscoincidedwith
has been found to respond to salinity: In rice, OsCLCa aNa+transporterrelatedtoOsHKT1;5inrice,andthisgene
was significantly upregulated in salt-sensitive cultivars in was shown to be responsible for removal of Na+ from the
response to salinity stress and OsCLCc, which is expressed xylem in the roots [49]. Members of the H+:monovalent
8 ISRNMolecularBiology
cationexchangerfamily(CHX)arealsolikelytocontribute of Na+ in the vacuole either through increased uptake or
to Na+ translocation. AtCHX21 is mainly expressed in the decreased efflux across the tonoplast. Several studies using
root endodermis, and loss of function in this gene reduced overexpressionofNHX andvacuolarpyrophosphatasehave
levels of Na+ in the xylem sap without affecting phloem shown this strategy to be effective (Table1) [11, 15, 93–
Na+concentrations[125].Inrice,salt-inducedexpressionof 96,98–100].
OsCHX11 in roots was cultivar dependant and higher in a
tolerantcultivar[126].Thedifferentialexpressioncorrelated
6.Conclusion
withahigherK+/Na+ratiointhetolerantcultivarsuggesting
that CHX11 may be involved in long-distance transport of Several abiotic stresses cause changes in morphological,
Na+and/orK+. physiological, biochemical, and molecular processes in
plants. The increasing prevalence of soil salinity is one of
5.EngineeringPlantSalinityTolerance themostdangerousobstaclestoimprovingcropproductivity
and quality. The adverse effects of saline soil include ion
Currently, a large number of potential gene targets are toxicity, nutrient constraints, osmotic stress, and oxidative
available to manipulate salt tolerance. This number has stress.Manygenetargetsinvolvedinsalttolerancehavebeen
drastically increased through the many large scale tran- identifiedthroughvariousapproaches,particularlythrough
scriptomic studies over the past decade, but in many transcriptomic studies. It is likely that such approaches
cases the validity of the reported findings has yet to be generate many false positives [136], and this is born out
established. For the various processes that contribute to by a lack of supporting evidence for an actual function
salt tolerance, regulating uptake of Na+ and Cl− from the in plant salinity tolerance. The accumulative data show
soil is of primary importance, particularly in glycophytes importance of two particular classes of transporters: HKTs
whichappeartohaveunidirectionalNa+andCl−influxthat which function in both Na+ uptake and long-distance
greatly exceeds net uptake [127]. Although several studies translocation [47] and NHXs in their capacity as Na+:H+
antiport [137] or by maintaining K+ homeostasis [138].
convincingly show that nonselective cation channels are
Thesignificanceofthesesystemsisoftenisoformdependent
involved, their molecular nature is largely unknown. Out
andmaybefurthercomplicatedbyallelicvariationbetween
of the substantial gene families that encode nonselective
cultivars. Manipulation of several of the genes discussed
cation channels (CNGCs and GluRs), only CNGC3 and
abovehasbeenshowntoalteruptake,efflux,translocation,
CNGC10 were shown to have a moderate impact on salt
and compartmentation of Na+. Knowledge gained through
tolerance [25, 128]. The data available suggest that single
use of heterologous expression systems and model plant
CNGCsdonotplayimportantrolesinNa+uptake.However,
systems provides an extremely useful starting point for
creatingmultiplelossoffunctionmutants,forexample,for
the development of salinity-tolerant crop plants. However,
allCNGCsorGluRsexpressedattherootperiphery,maybe
further work involving the transgenic expression of Na+
requiredtoprovidemoreconclusiveevidenceinthisrespect.
transporters in cereal and broad leaved crop plants needs
Na+effluxprocessesshouldbemaximizedtocounteractNa+
to be undertaken. Before any claims of salinity tolerance
influx. This might be possible by overexpressing Na+/H+ can be substantiated, robust data on yield measurements is
antiporters or Na+-ATPases specifically in the outer root required; preferably from field-based trials [139]. Also, it is
cellstoimproveNa+extrusion.ThebryophytePhyscomitrella arguedthatphenotypingofArabidopsisshouldbecarriedout
patens is tolerant to a range of stresses and is consequently underthemostrelevantconditionspossible,notably,under
attractingsignificantattentionasapotentialsourceofgenes transpiringconditionsratherthaninsealed-agar-plate-based
toimprovestresstoleranceinhigherplants[129–132].Asin assays,astranspirationisacrucialfactorinthetransportof
manyalgaeandfungi[133],andunlikehigherplantsthatdo ionssuchasNa+throughtheplant.
nothaveprimaryATPhydrolysingNa+pumps,P.patenshas
two Na+-ATPases: PpENA1 and PpENA2 [134]. Expression
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